Broadening the Spectrum of Diffusion Weighted Imaging to Evaluate Marrow Pathologies

Razak K and Meena GL*
Department of Radiodiagnosis, S.P. Medical College, India
*Corresponding author: Meena GL, Senior Professor, Department of Radiodiagnosis, Sardar Patel Medical College, Bikaner, Rajasthan, India
Submission: August 03, 2018; Published: August 27, 2018
Broadening the Spectrum of Diffusion Weighted
Imaging to Evaluate Marrow Pathologies
Introduction
Diffusion-weighted whole-body imaging with background
body signal suppression (DWIBS), which is also called whole body
diffusion-weighted imaging (WB-DWI) [1], has been used for
screening bone marrow diseases [2], tumor staging, monitoring,
and predicting tumor response to therapy [3]. For a correct
interpretation,thesignalcharacteristicsofnormalbiologicaltissues
should be known to better differentiate normal from abnormal
tissues. However, the signal characteristics of normal adult bone
marrow in diffusion-weighted (DW) images has not been clearly
depicted in the literature. To the best of our knowledge, few papers
have studied this topic. Ording Muller et al. [4] studied the WB-DWI
(b=1000 s/mm2
) signal features of bone marrow in the normal
lumbar spine and pelvis of 42 children (24 boys, 18 girls; age range,
2 months-16 years) by visual evaluation. High signal intensities
both within the vertebral bodies and pelvic skeleton were observed
in all children. Two papers indicated that the normal bone marrow
apparent diffusion coefficients (ADC) were negatively correlated
with age (0-84 years) [5,6], but one paper did not support the
relationship in 53 male participants aged 28-82 years [7]. In clinical
practice, visual assessment of signal intensity on DW images is
commonly used for diagnosis rather than ADC measurements.
However, no literature depicts the DW signal intensity as related to
age and gender in normal adults. The purposes of our study were to
evaluate the signal characteristic of normal adult bone marrow on
WB-DWI as related to age and gender and to determine the causes
of the adult bone marrow signal characteristics related to age and
gender.
Material and Methods
Participant selection
Thisprospectivestudywasapprovedbyourinstitutionalreview
board and informed consent was obtained from all participants.
From October 2016 to March 2017, 100 healthy volunteers were
enrolled in this study, with
a. Inclusion criteria including:
(i) Normal laboratory examinations (including blood count
and clotting time test)
Research Article
Researches in Arthritis &
Bone StudyC CRIMSON PUBLISHERS
Wings to the Research
1/7Copyright © All rights are reserved by Meena GL.
Volume 1 - Issue - 2
Abstract
Objectives: To evaluate the signal characteristics of normal adult bone marrow in whole-body diffusion-weighted (DW) images (WB-DWI), to
correlate these characteristics with age and gender, and to determine the causes of these phenomena.
Material and Methods: Ninety-eight healthy volunteers underwent WB-DWI (b=0 and 800s/mm2). Two radiologists visually evaluated the
signal characteristics of bone marrow in DW images separately. One radiologist measured the apparent diffusion coefficient (ADC) of the thoracic and
lumbar vertebrae, bilateral femur (including head, neck, and proximal and distal femoral shaft), bilateral humeral head, ilium, and scapula. The signal
characteristics of normal bone marrow were analyzed.
Results: The visual evaluation results of DW images indicated that hyperintensity of bone marrow was more frequently seen in women aged 21-
50 years (68.4%) than in men aged 21-50 years (3.3%) (P <0.001), men aged 51-81 years (5.9%) (P<0.001), and women aged 51-81 years (15.4%)
(P=0.001). However, no statistically significant difference was found between men and women aged 51-81 years (P=0.565). The ADC of bone marrow
was significantly higher in women than in men aged 21-50 years. Bone marrow ADC showed significant negative correlation with age in women but
not in men.
Conclusion: The signal intensity of bone marrow varies with age and gender in DW images. ADC and the T2 shine through effect contributed to the
bone marrow signal intensity in DW images, and the latter effect may predominate.
Keywords: Marrow; Pathologies; Imaging; Diffusion; Adults

Res Arthritis Bone Study Copyright © Meena GL
2/7How to cite this article: Razak K, Meena G. Broadening the Spectrum of Diffusion Weighted Imaging to Evaluate Marrow Pathologies. Res Arthritis Bone
Study. 1(2). RABS.000509.2018.
(ii) No known clinical or imaging evidence of any bone disease
(such as tumor, metastases, or metabolic disorder)
(iii) No history of surgery or injury
(iv) No history of smoking
(v) No history of chemotherapy or radiotherapy and
(vi) No contraindication to magnetic resonance (MR)
examination.
b. Exclusion criteria included:
(i) Any confirmed abnormality of bone marrow in the current
MR examination
(ii) History of alcoholism and certain hormonal therapy and
(iii) Suboptimal image quality.
Two participants were excluded from further analysis because
of the suboptimal DW image quality. After exclusion, 98 healthy
volunteers (51 women; age range, 21-78 years; 47 men; age range,
24-81 years) were included for this study. The participants were
divided into four groups based on age (21-30, 31-40, 41-50, and
51-81 years) according to another paper [8].
MR examination
All images were acquired on a 1.5-Tesla magnetic resonance
scanner (Magnetom Avanto, Siemens, Erlangen, Germany) with a
45mT/m maximum gradient capability and one 12-element head
matrix coil, one 4-element neck matrix coil, one 24-element spine
matrix coil, and four 6-element body matrix coils (Siemens, Munich,
Germany). The protocol included a coronal T2-weighted (T2W)
short TI inversion recovery (T2-STIR) and an axial DW single-shot
echo-planar imaging (EPI) sequence. The parameters of the T2-
STIR sequence were: TR/ TE/TI, 4000/322/150ms; field of view
(FOV), 50 50cm2
; slice/gap, 4/0 mm; matrix, 256 256; number of
signals acquired, 1. Coronal images were acquired from the head to
the knee using the 4-station approach. Images at the slice level from
each station were spliced into coronal whole-body images using
software available on the MR workstation (Syngo VB15; Siemens).
The parameters of the EPI sequence were: TR/TE, 8000/83ms;
FOV, 50 50cm2
; slice/gap, 4/0mm; matrix, 192 192; number of
signals acquired, 6; b values, 0 and 800s/mm2
. Axial slices were
acquired from head to knee using the 5-station approach. Each
station included 60 slices with a range of 240mm, covering a total
range of l200mm. Scanning time for each station was 3 min 26s.
Coronal maximal intensity projection (MIP) images of DW images
were reconstructed with original axial images and with inverted
images for background suppression. Quantitative ADC maps were
automatically generated by the MR system.
Image evaluation
Two types of image evaluation were performed: a qualitative
visual evaluation of the DW (b=800s/mm2
) image to determine
bone marrow signal intensity and a quantitative ADC measurement
of bone marrow in the axial ADC map at a workstation. Visual
evaluation of bone marrow signal intensity was performed by
radiologists with 20 years and 3 years of clinical experience
interpreting musculoskeletal MR images. Prior to the visual
evaluation, an overview of all images was performed to evaluate
bonemarrowimagequality.Thebonemarrowsignalintensityofthe
DW images was defined on a two level ordinal scale, ‘‘hypointense
or isointense’’ and ‘‘hyperintense’’ based on the literature [1,4].
Bone marrow is defined as hypointense or isointense (Figure 1a &
1b) when it has a signal intensity that is lower than or equal to the
signal intensity of fat and muscle. Hyperintense (Figure 1c & 1d)
is defined as having higher signal intensities than fat and muscle.
Visual interpretation by the two radiologists was based on the
bone marrow in the entire body. All images were independently
evaluated by each of the two radiologists who were blinded to the
findings of the other. To assess intra-observer agreement, reader
1 re-evaluated the DW images for all 98 participants following
the procedure used in the first evaluation 1 month later without
knowledge of the results of the first reading. For clarity, only
the results from reader 1 in the first evaluation are reported. To
effectively double blind qualitative findings, all data were collected
by the third radiologist (FZC) after completion of the evaluation.
The quantitative measurements of ADC of bone marrow were
performed by one radiologist (FZC) using commercially available
software (Syngo VB15; Siemens) using the following methods:
In the vertebrae, one circular region of interest (ROI) (thoracic
vertebrae, 21 pixels; lumbar vertebrae, 40 pixels) was placed by
identifying a central slice in each of the five thoracic vertebrae (T12
through T8) and each of the five lumbar vertebrae (L1 through L5),
respectively (Figure 2a & 2b). The average ADC of five vertebrae
was used for further analysis. In the femoral head, femoral neck,
humeral head, and scapula, specific sized ROIs with 65, 21, 65, and
5 pixels, respectively, were placed on five central consecutive slices
of each side. In the proximal femoral shaft, ROIs with 21 pixels
were placed on five consecutive slices below the femoral greater
trochanter. In the distal femoral shaft, ROIs with 24 pixels were
placed on five consecutive transverse image slices at the distal
end of the femur. In the ilium, ROIs with 12 pixels were placed on
five consecutive slices at the sacroiliac joint level of each side. The
average ADCs of both sides of five consecutive slices in the above
each anatomy site were used for further analysis. Care was taken
to exclude blood vessels, cortex, and artifacts from the ROI. These
ROIs were manually set on axial EPI images acquired with b=0s/
mm2
, allowing these structures to be easily identified, then copied
onto axial ADC maps. The software automatically calculated ADC by
averaging the signal intensity within the ROI. The measurements
were repeated using the same methods as the above by FZC 1 month
later without reference to the previously determined values for the
intra-observer reliability test. The values of the first measurement
for each site were used for further analysis.
Statistical analysis
The frequency of hyperintense bone marrow in the DW images
of women aged 21-50 years and men aged 21-50 years or 51-81
years, and women aged 51-81 years were compared using the 2
test. For men and women aged 51-81 years, the comparison was
made using Fisher’s exact test because the total number of the

Study. 1(2). RABS.000509.2018.
participants in this age group was less than 40. To compare the ADC
values of bone marrow between male and female participants in
different age groups and between women aged 21-50 and 51-81
years at various bone sites, Student’s t-test was used for data with
normal distributions, while for data without normal distributions,
the Mann-Whitney U test was used. Spearman’s rho was calculated
to assess the relationship between the ADC values and age at
various bone sites in female and male participants. Intra-observer
and inter-observer agreement in the qualitative bone marrow signal
intensity visual evaluation were analyzed using weighted Cohen’s
kappa statistics. The strength of agreement was interpreted on the
basis of the k values suggested by [9], as adapted from the method
of [10], as follows: k less than 0.20, poor; k of 0.21-0.40, fair; k of
0.41-0.60, moderate; k of 0.61-0.80, good; and k of 0.81-1.00, very
good agreement Intra-observer reliability of ADC measurements
was determined using intraclass correlation coefficients (ICCs).
ICC values of 0.41-0.60 indicated moderate; 0.61-0.80, good; and
0.81 or greater, very good agreement [11]. All statistical analyses
were performed using commercial software SPSS 13.0 (SPSS Inc.,
Chicago, IL, USA). All tests were two-sided with a significance level
of P< 0.05.
Figure 1: Normal bone marrow appearance of healthy volunteers on WB-DWI. (a, b) A 24-year-old man. All bone marrow shows
as hypo- or isointense on the maximal intensity projection image of the WB-DWI (a) and by inverted image (b). (c, d) A 25-year-old
woman. Bone marrow shows as hyperintense on the maximal intensity projection image of WB-DWI (c) and by inverted image (d).
Figure 2: Images of a 27-year-old woman. ROI was manually drawn on the axial DW image (b=0s/mm2) (a) and was automatically
copied onto the corresponding ADC map (b).
Results
Visualization of signal intensity of bone marrow on DW
images (b=800s/mm2
)
The bone marrow showed hyperintense signals in 30
participants (2 men, 28 women) and hypo- or isointense signals
in the remaining 68 participants based on visual inspection of the
DW images. The age and gender distributions of the participants
with hyperintense bone marrow are shown in Table 1. The visual
evaluation results indicated that hyperintense bone marrow was
more frequently seen in women aged 21-50 years (68.4%) than
men aged 21-50 years (3.3%) or 51-81 years (5.9%), or women

Study. 1(2). RABS.000509.2018.
aged 51-81 years (15.4%). However, no statistically significant
difference was found between men and women aged 51-81 years
(Table 1) (Figure 3).
Table 1: Age and sex distribution of participants whose
bone marrow was hyperintense in the DW images (b=800s/
mm2
).
Age Range
(Years)
Men (n) Women (n) Χ2
p
21-50 1(30) 26(38)*† 29.666 <0.001
21-50 0(7) 10(11)
31-40 1(8) 5(8)
41-50 0(15) 11(19)
51-81 1(17) 2(13) 0.739 0.565
The numbers in parentheses are partic-
ipant numbers within each age and sex.
*Statistically significant differences were also found be-
tween the 21-50 and the 51-81 year-old female groups
(Χ2
=11.004, p=0.001).
†
Statistically significant differences were also found
between the 21-50 -year-old female group and the 51-81
-year old male group (Χ2
-18.381, p=0.000)
Comparison of the ADC values between the genders of
different age groups
In the 21-50-year age group, the ADC values of bone marrow
were significantly higher in women than in men in all of the regions
that were measured (Table 2). The ADC values of bone marrow in
the 21-50-year age group were significantly higher than those in
the 51-81-year group of women in all regions except for the distal
femur segment and the scapula.
Table 2: Comparison of ADC values (×10-3
mm2
/s) of bone marrow for different age and sex at various bone sites.
Region
21-50 Years 51-81 Years
Men Women p Men Women p
Thoracic vertebrae 0.51±0.06 0.61±0.06 <0.001* 0.51±0.08 0.53±0.06 0.436*
Lumbar vertebrae 0.49±0.06 0.60±0.05 <0.001* 0.47±0.07 0.52±0.06 0.042*
Head of femur 0.22(0.07) 0.34(0.11) <0.001† 0.27(0.09) 0.29(0.08) 0.028†
Neck of femur 0.31(0.11) 0.57(0.13) <0.001† 0.33±0.11 0.36±0.11 0.439*
Superior segment of femur 0.66±0.15 0.84±0.10 <0.001* 0.66±0.12 0.76±0.07 0.013*
Distal femoral shaft 0.22(0.16) 0.33(0.14) 0.001† 0.24(0.21) 0.25(0.14) 0.305†
Ilium 0.47±(0.11) 0.54±0.08 0.007* 0.45(0.18) 0.49(0.15) 0.983†
Head of humerus 0.28(0.11) 0.43(0.21) 0.000† 0.25±0.07 0.97±0.09 0.001*
Scapula 0.47±0.10 0.54±0.08 0.001* 0.41±0.11 0.49±0.09 0.031*
*Values are mean±SD for data with normal distributions. Student’s t-tests was used, and statistical significance was
set at p<0.05.
†
Values are the median and interquartile range for data without normal distributions. The Mann-Whitney U test was
used, and statistical significance was set at p<0.05.
Figure 3: Age and sex distribution of participants whose bone marrow showed as hyperintense on DW images (b=800s/mm2).

Study. 1(2). RABS.000509.2018.
Correlations between the ADC values of bone marrow
and age for all female and male participants
There were significant negative correlations between the ADC
values of bone marrow and age for women in all regions except for
the distal femur segment and the scapula. In the scatter diagram,
for participants older than 50 years, the tendency is not very
strong compared with the 21-50-year-old participants (Figure 4).
However, there were no significant correlations between the ADC
values of bone marrow and age in all the regions in men (Table 3).
Table 3: Spearman’s rho analysis of the ADC values and
ages in various regions for male and female participants.
Region
ADC Values and Ages
Men Women
Thoracic vertebral 0.112(0.453) -0.549(<0.001)*
Lumbar vertebral -0.027(0.858) -0.629(<0.001)*
Head of femur 0.131(0.379) -0.329(0.018)*
Neck of femur -0.094(0.531) -0.524(<0.001)*
Superior segment of femur 0.095(0.523) -0.338(0.015)*
Distal femoral shaft 0.023(0.878) -0.119(0.406)
Ilium 0.039(0.796) -0.548(<0.001)*
Head of humerus -0.227(0.125) -0.416(0.002)*
Scapula -0.173(0.244) -0.167(0.241)
Data are correlation coefficients with the p values in pa-
rentheses.
*Denotes significant correlation; no*denotes no significant
correlation.
Intra- and inter-observer agreement for visual evalua-
tion of the signal intensity of the DW images
In the visual evaluation of the signal intensity of the DW images,
inter-observer agreement (k=0.861) and intra-observer agreement
of reader 1 (k=0.885) were very good.
Intra-observer reliability of the ADC measurements
In the quantitative ROI assessment, the intra-observer
reliability of ADC measurements of all regions was good to very
good (ICC=0.715-0.865).
Discussion
We found that, in the DW images, the bone marrow of women
aged21-50years(68.4%)wasoftensignificantlymorehyperintense
than the 21-50 and 51-81- year-old male groups (3.3% and 5.9%,
respectively), and the 51-81-year-old female group (15.4%). There
was no significant difference between women (15.4%) and men
(5.9%) older than 50 years. These results suggest that men older
than 21 years or women older than 50 years with bone marrow
that is hyperintense in WBDWI should be further examined by
laboratory tests or other tests to rule out bone marrow disease. We
found that bone marrow ADC in women was negatively correlated
with age. This tendency is more obvious and statistically significant
in women aged 21- 50 years than in those aged more than 50 years,
which is shown in a scatter diagram of lumbar vertebral bone
marrow (Figure 4). Nonomura et al. [12] found that the ADC values
of bone marrow decreased as fat increased based on biopsies of iliac
crest bone marrow. The reason for this behavior may be that the fat
cells have limited room due to less intracellular water and adjacent
free water, which limit molecular diffusion. Shih et al. [13] found
that vertebral marrow fat content increased with increasing age in
women, which could explain the negative relationship between ADC
and age in women in our results. Vertebral marrow fat content for
men increases slowly throughout life [8,14], and the water fraction
of vertebral marrow for men was found to be relatively stable over
the age range of 25-75 years [15], which means marrow conversion
was almost complete for men by the age of 25 years. These results
may explain the lack of correlation of bone marrow ADC and age
for men in the current study, which is consistent with the result
of another study [7]. According to our results, the ADC values of
bone marrow were significantly higher in women than in men aged
21-50 years. The bone marrow signal intensity in DW images of
women was also higher than that of men in this age group. However,
the literature indicates that structures with restricted diffusion
are subject to less signal attenuation, making the signal intensity
higher in the DW images and giving lower ADC values on ADC maps
[16]. This contradiction may be explained by the fact that the bone
marrow with higher ADC values has less fatty marrow and more
water, which results in tissue with longer T2 relaxation times. The
longer T2 relaxation time can increase the signal intensity in the
DW images, which is called the T2 shine through effect [17-20].
Because the signal intensity of the DW images is mainly affected
by ADC and the T2 shine-through effect and, by a smaller amount,
the proton density [17], we speculate that if the magnitude of the
positive contribution from the T2 shine-through effect is greater
than the magnitude of the negative contribution from the increased
ADC, the net effect of both contributions will be positive in DW
images. One paper supports our results that the water fraction of
the lumbar vertebral marrow for women exceeded that for men
aged 25-54 years [15], which could explain the higher bone marrow
signals of women aged 21-50 years in the current study, i.e. due to
the T2 shine through effect. The marrow ADC in women aged 21-
50 years was higher than in men aged 21-50 years, which implies
that there is more hematopoietic marrow and less fatty marrow
[8,14,21] in women than in men at this age. In this period, women
have much higher estrogen than men because the average natural
menopause age for Chinese women usually begins close to the
age of 50 years [22]. Estrogen levels have a negative influence on
the levels of marrow fat [23], which can explain the above results.
After a precipitous drop around menopause, estrogen levels in
postmenopausal women are slightly lower than those in men,
whereas estrogen levels remain virtually unchanged for men with
increasing age [24]. This behavior may be the cause of the high
signal in the DW images and the ADC values that are almost the
sameinwomenasmenagedover50years.However,themechanism

Study. 1(2). RABS.000509.2018.
of estrogen affecting bone marrow fat is still not clear. Apart from
estrogen, growth hormone [25] and testosterone [26] also affect
the bone marrow fat component, which make the scenario complex
and further study is needed. Because chronic anemia could lead to
yellow marrow changing to hematopoietic marrow [27], we suspect
that menses, which can induce blood loss, can affect the proportion
of hematopoietic and fatty marrow. However, there is no reliable
evidence that supports this conjecture. Our study had several
limitations. First, the volunteers were of heterogeneous ages. The
populations of some age groups were relatively small, which may
skew the results. Second, participants in the age range of 0-20 years
were not included in the study, so further study is needed. Third,
other factors that may affect bone marrow, such as starvation [28],
bone mineral density [29], body mass index [30], physical activity,
vitamin D levels, menstrual status, and sex hormones [31,32], were
not taken into consideration.
Figure 4: Scatter diagram indicating the correlation between the ADC (10-3mm2/s) of the lumbar vertebral bone marrow and
age for female participants, r=-0.629.
Conclusion
In conclusion, we demonstrated the signal characteristics of
normal adult bone marrow in WB-DWI and correlated them with
age and gender. Knowledge of these factors is essential to correctly
interpret DW images in clinical practice.
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